Vitamin E Supplementation Increases the Attractiveness
of Males’ Scent for Female European Green Lizards
Rena ´ta Kopena1,2, Jose ´ Martı ´n2, Pilar Lo ´pez2, Ga ´bor Herczeg1,3*
1Behavioural Ecology Group, Department of Systematic Zoology and Ecology, Eo ¨tvo ¨s Lora ´nd University, Budapest, Hungary, 2Departamento de Ecologı ´a Evolutiva,
Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Cientı ´ficas, Madrid, Spain, 3Ecological Genetics Research Unit, Department of Biosciences,
University of Helsinki, Helsinki, Finland
Background: In spite that chemoreception is important in sexual selection for many animals, such as reptiles, the
mechanisms that confer reliability to chemical signals are relatively unknown. European green lizards (Lacerta viridis) have
substantial amounts of a-tocopherol (=vitamin E) in their femoral secretions. Because vitamin E is metabolically important
and can only be attained from the diet, its secretion is assumed to be costly. However, its role in intraspecific
communication is unknown.
Methodology/Principal Findings: Here, we experimentally show that male European green lizards that received a dietary
supplement of vitamin E increased proportions of vitamin E in their femoral secretions. Furthermore, our experiments
revealed that females preferred to use areas scent marked by males with experimentally increased vitamin E levels in their
secretions. Finally, female preferences were stronger when vitamin E differences between a pair of males’ secretions were
Conclusions/Significance: Our results demonstrate that female green lizards are able to discriminate between males based
on the vitamin E content of the males’ femoral secretions. We suggest that the possible cost of allocating vitamin E to
secretions, which might be dependent on male quality, may be a mechanism that confers reliability to scent marks of green
lizards and allows their evolution as sexual signals.
Citation: Kopena R, Martı ´n J, Lo ´pez P, Herczeg G (2011) Vitamin E Supplementation Increases the Attractiveness of Males’ Scent for Female European Green
Lizards. PLoS ONE 6(4): e19410. doi:10.1371/journal.pone.0019410
Editor: Stephen R. Proulx, UC Santa Barbara, United States of America
Received January 6, 2011; Accepted March 31, 2011; Published April 28, 2011
Copyright: ? 2011 Kopena et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by the Spanish Ministerio de Ciencia e Innovacio ´n (MCI-CGL2008-02119/BOS), the Hungarian-Spanish Intergovernmental
SandT Cooperation Programme (HH2006-0024), and the Hungarian Scientific Research Fund (OTKA-F68403). The funders had no role in study design, data
collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: email@example.com
Theoretical models predict that sexual signals can only be
evolutionarily stable if they are honest, i.e., condition dependent
and costly to the signaler, and if the signal’s cost is correlated with
the signaler’s quality (e.g. [1–2], but see [3–5] for more complex
scenarios). Production of chemical signals may be energetically
costly, especially if chemicals cannot be produced by the animals
themselves, but have to be acquired from food [6–7]. Such
chemical signals can be used as ‘honest signals’ (sensu ) or
‘revealing indicators’ (sensu [9–10]), which provide reliable
information, as they would accurately reflect the signaler’s ability
to exploit resources . Chemical signals of territorial animals
can have further ecological costs : (i) time and energy
investments to depositing and maintaining the signals and (ii) the
increased of risk of predation and parasite infection during
deposition and maintenance.
Irrespective of the costs, chemical signals play an important role
in intraspecific communication and sexual selection of a wide array
of taxa and contexts (e.g. [6,12–15]). In lizards, pheromonal
detection is often based on femoral gland secretions ([16–18]
reviewed in ), which may be used in sexual selection [7,18–20].
Behavioral experiments suggested that femoral gland secretions
might transmit information about a male’s quality, and thus females
may use this information to choose their mates [7,19,21–22].
However, the chemical composition of gland secretions is rarely
studied , and the mechanisms that could confer reliability to
chemicals as sexual signals remain poorly understood.
Different species of so-called ‘green lizards’ have substantial
amounts of a-tocopherol (=vitamin E) in their femoral secretions
(Lacerta schreiberi ; L. viridis ; L. lepida ). Vitamin E
consists of a group of isoprenoid compounds of plant origin that
are the main lipophilic antioxidants and radical scavengers
involved in membrane defense, and that also have immunostimu-
latory activity [27–29]. Secretion of vitamin E is assumed to be
costly for lizards: a-tocopherol is typically produced by microor-
ganisms and plants, and thus it should be of dietary origin .
The physiological relevance of vitamin E and the severe
pathological consequences of its deficiency, such as neurological
disorders or lung diseases, together with its dietary origin impose a
major challenge for sustaining an adequate supply of this vitamin
to different tissues . Because vitamin E is important
metabolically, it should only be allocated to femoral secretions
when it is in abundant supply.
PLoS ONE | www.plosone.org1 April 2011 | Volume 6 | Issue 4 | e19410
We tested the hypothesis that high levels of vitamin E in femoral
secretions of male European green lizards (L. viridis) might be a
sexual trait preferred by females. We supplemented experimental
males with dietary vitamin E, and examined (i) whether the
treatment changed the characteristics of their femoral secretions,
(ii) whether females were more attracted to areas scent marked by
supplemented than non-supplemented control males, and (iii) if the
strength of females’ preferences were related to the magnitude of
differences in vitamin E levels between males offered. We
predicted that vitamin E supplementation will enrich the vitamin
E content of male European green lizards’ femoral secretions, that
females will prefer males with more vitamin E in their secretions,
and that the strength of female preference is positively correlated
with the vitamin E level difference between the offered male
Experiments were performed according to the guidelines of the
Hungarian Act of Animal Care and Experimentation (1998,
XXVIII, section 243/1998), which conforms to the regulation of
animal experiments by the European Union. The experiment was
done under the license of the Middle-Danube-Valley Inspectorate
for Environmental Protection, Nature Conservation and Water
Management (No. 21765/2007). All animals were returned
healthy to their capture sites at the end of the experiment.
We used noosing to capture 36 adult European green lizards (16
females and 20 males) at the beginning of April 2007, before the
start of their mating season, near Ta ´pio ´szentma ´rton (Pest County,
Hungary; 47u209N, 19u479E). The habitat is sand ‘puszta’ with
disturbed grassland, honey locust (Gleditsia triacanthos) scrub, and
black pine (Pinus nigra) forest patches. Only adult lizards with intact
or fully regenerated tails were considered.
Lizards were transported to the Zoological Institute of the Szent
Istva ´nUniversity,and housed
70640650 cm (length, width, and height, respectively) plastic
terraria. Lizards were fed mealworms and crickets and water was
provided ad libitum. Terraria of males and females were in different
rooms to avoid any contact between them before trials. The room
temperature was roughly constant (28uC) and the photoperiod was
held natural (approx. 14L:10D).
Vitamin E supplementation
We made the experiments in May 2007. We paired males (10
pairs) based on their snout-to-vent length (maximum difference
was 0.6 mm). One male of each pair was assigned randomly to the
supplement treatment, and the other to the control treatment.
Supplemented males (S-males) received daily, during 21 days,
0.04 ml of vitamin E supplement (synthetic (6)-a-tocopherol;
purchased from Sigma-Aldrich Chemicals Co.), which contained
97% of synthetic vitamin E (approx. 1014 IU ml21) and 3%
soybean oil (with approx. 0.32 IU ml21of natural vitamin E, i.e.
D-a-tocopherol). Thus, we provided S-males with approximately
40.5 IU of vitamin E per dose. While this dose is above the daily
minimal physiological necessity of vitamin E for reptiles of this
size, it is still well below the tolerable upper intake leves [30,32–
33]. To ensure that all lizards swallowed the entire dose, we gently
handled lizards and used sterile plastic syringes with a canula to
deliver slowly the solution into their mouth. Control males (C-
males) were handled in the same way as S-males, but we
administered them 0.04 ml of distilled water instead of the vitamin
supplement to avoid any unwanted vitamin E intake. Therefore,
the soybean oil in the diet also varied between treatments.
However, as all experimental animals were fed ad libitum, we
believe that the very small amount of supplemented oil per se could
not have an effect on the quality or quantity of the males’
Chemical analyses of male femoral secretions
At the end of the experiments, we collected femoral secretion of
males directly into glass vials with Teflon-lined stoppers that were
stored at 220uC. Samples were analyzed by gas chromatography-
mass spectrometry (ThermoQuest Trace 2000) equipped with a
Supelco-Equity-5 column temperature programmed (50–280uC at
5uC/min and 280uC for 30 min). Compounds were identified by
comparison of mass spectra in the NIST library, and later
confirmed with authentic standards (see  for details of analyses
and chemicals in secretions). The relative amount of each
component was determined as the percent of the total ion current
(TIC) area transformed following Aitchison’s formula :
[Zij,=ln (Yij/g(Yj)], where Zijis the standardized peak area i for
individual j, Yijis the peak area i for individual j, and g(Yj) is the
geometric mean of all peaks for individual j (for similar analyses see
). Then, we calculated the relative proportions of the different
types of chemicals in secretions (alcohols, fatty acids, lactones,
steroids, squalene, and a-tocopherol; see ). To test for
differences in relative proportions of chemicals in secretions of
S- and C- males, we ran a multivariate General Lineal Model
(GLM) with transformed areas of alcohols, fatty acids, lactones,
steroids, squalene, and a-tocopherol (=vitamin E). Then, because
we found a significant result in the multivariate analyses (see
results), we could perform protected GLMs separately on each
chemical or groups of chemicals, to test which one changed more
with the diet supplementation and explained the significant
difference found in the previous multivariate GLM model .
Following the significant findings (see Results), we also ran a
repeated measures GLM using a-tocopherol (=vitamin E)
proportions as the dependent variable, and male treatment (S vs.
C) within the size-matched pairs (see above) used in the preference
tests as a repeated measures factor.
Female preference tests
During the last week of the experimental supplementation, we
placed eight absorbent paper stripes (6640 cm) on the floor of
males’ terraria, and left them there to obtain the scents from
femoral secretions of each male. Food was not deposited on the
papers to avoid odor contamination. During this week, S-males
were still receiving the supplement of dietary vitamin E and C-
males the water.
Female preference tests were performed at the end of this
exposition period. Females’ plastic terraria (70640650 cm,
length, width, height, respectively) had three water dishes and
three cardboard shelters that also acted as basking places, two
placed symmetrically at each end of the cage and one in the
centre. We tested all females with five different male pairs in five
consecutive days. We chose male pairs and females randomly, but
in a way that every male pair was tested eight times with different
females and every female met five different pairs of males. At the
beginning of each experiment (0800 h GTM), when females were
still inactive, we took a paper strip from each of the two males
from a given pair (one C-male and one S-male matched in size; see
above) and fixed their strips on alternate ends of the female’s
terraria (side was chosen randomly). Paper strips were handled
with fresh gloves to avoid contamination with human odor.
Vitamin E as a Sexual Signal in Lizards
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Females were monitored every 10 min from a concealed view
point and their locations (determined by the head position) in the
terraria were recorded from 0900 to 1400 h GTM. We divided
terraria into three equally-sized parts: two terminal parts where
scent-marked papers were located, and a central ‘neutral’ part. We
excluded trials where females (i) were observed only in one area or
(ii) were located in the area of each male’s scent less times than on
the area of the other male and the neutral area together, to ensure
that females were exposed to both males’ tiles and were aware of
both male’s stimuli, and to avoid trials were females might be
stressed by the setup and did not respond.
We analyzed the outcome of the female preference tests with
Generalized Linear Mixed Models (GLMMs) with binomial error
and logit link. First, we ran a GLMM with the proportion a certain
female was observed at a certain male’s side (N observations=30,
see above) as dependent variable, treatment (supplemented vs.
control) and the identity of both the females and the male pairs as
fixed factors, and trial (the experiment including a certain male
pair and a certain female) as random factor. Second, we ran
another GLMM to test whether the strength of female preference
was related to the vitamin E difference within a given male pair.
Here, we used the mean of the proportions of female observations
at a certain male’s area (every male pair was assessed by several
females) as dependent variable, the vitamin E concentration in the
given male’s secretion as a continuous fixed effect, and male pair
as random factor. We note that we also ran two simple repeated
measures GLMs built similarly to the two GLMMs above, but
with the arcsine-squareroot transformed proportion of female
observations as dependent variable, and male treatment (S vs. C)
within the size-matched pairs as repeated measures factor. These
models revealed qualitatively similar patterns to the GLMMs (data
Chemicals in femoral secretions
After the experimental supplementation, chemicals found in
femoral secretions of both groups of males were qualitatively similar
(i.e., the samechemical compounds were found in secretions of both
C- and S-males), but S-males had secretions that differed in relative
proportion of chemicals from those of C-males (multivariate GLM,
Wilks’l=0.18, F6,13=9.71, P,0.001). However, these differences
were only explained because S-males had significantly higher
proportions of a-tocopherol (=vitamin E) (GLM, F1,18=15.48,
males=5.6760.12; C-males=4.8660.12). In contrast, there were
no significant differences between S- and C-males in proportions of
alcohols (F1,18=0.01, P=0.93), fatty acids (F1,18=0.81, P=0.38),
lactones (F1,18=1.06, P=0.32), steroids (F1,18=2.83, P=0.11) or
squalene (F1,18=1.68, P=0.21). Therefore, the experimental
supplementationonly affected to contents of vitaminE in secretions,
which were otherwise similar between treatments in their chemical
composition and proportion of chemicals.
In addition, if we compared differences in vitamin E content
between the S- and C-male within each pair, we also found a
significant difference (repeated measures GLM, F1,9=40.84,
P,0.001). However, the variation in vitamin E differences within
male pairs was considerable (range of differences in TIC
transformed areas=0.17–1.24), probably due to individual differ-
ences in initial proportions of vitamin E in the males of a pair.
Female preference tests
Our first GLMM revealed that the treatment effect was male pair
dependent (treatment: F1,36,0.01, P.0.99, male pair: F9,36=0.11,
P.0.99, female: F14,36=0.08, P.0.99, treatment6male pair:
F9,36=3.60, P=0.003, treatment6female: F14,36=1.51, P=0.16).
Removal of the nonsignificant effects including the factor ‘female’
resulted in a significant treatment effect while retaining the
P=0.0012, male pair: F9,50=0.07, P.0.99, treatment6male pair:
F9,50=2.29, P=0.031). Females were observed more times in the
areas of vitamin E supplemented males than in the areas of control
males; however, the effect varied among male pairs (Figure 1).
Further, our second GLMM revealed that the attractiveness of a
certain male’s area depended on the vitamin E concentration
difference of the males’ femoral secretion within a pair (F1,18=9.17,
P=0.007): larger difference resulted in stronger preference
Our results supported our predictions: (i) dietary vitamin E
supplementation increased the vitamin E proportions in the
femoral secretions of male European green lizards, (ii) female
lizards were spatially associated to the scent of vitamin E
supplemented males, and (iii) the strength of female preference
was positively correlated to the vitamin E level differences between
the offered scents of supplemented vs. control males.
The effect of dietary vitamin E supplementation on the femoral
secretions’ composition suggests that lizards with higher quality
diets are able to divert more vitamin E from metabolism into their
chemical signals. This, together with the fact that a-tocopherol is
of dietary origin suggests that allocation of vitamin E to secretions
might be costly and dependent of male quality. The nutritional
condition of males also affects the attractiveness of their
pheromones to females in some insects [37–38], and vitamin D
supplementation increased the quality of femoral secretions in
Iberian rock lizards (L. monticola ).
Female European green lizards showed clear preference to use
areas scent marked by males with more vitamin E in their
secretions, especially when the vitamin E divergences between
available scents were large. The reported female preference may
be explained by at least four ways. First, females might directly
use this male trait (i.e., higher levels of vitamin E) as a reliable
Figure 1. Female preference for male scent. The proportion
unmated female lizards (see text for details) were observed at the areas
containing chemical cues from size-matched vitamin E supplemented
vs. control male European green lizards. Means for every male pair (6
SE) are shown.
Vitamin E as a Sexual Signal in Lizards
PLoS ONE | www.plosone.org3 April 2011 | Volume 6 | Issue 4 | e19410
advertisement of male quality, because higher levels of vitamin E
in secretions may, for example, be correlated with the quality of
the immune systems of males, as it occurs in another green lizard
species (L. lepida; ). Second, females might use this trait
indirectly to estimate the quality of the males’ territory (i.e.,
quality of available food). Hence, females may use the
performanceof males as public
assessment . Third, females might not directly use vitamin
E levels as signals, but simply prefer scent marks with high
vitamin E levels because vitamin E is an antioxidant that would
increase duration and intensity of information provided by other
chemicals in secretions , which might include other actually
signaling chemicals. Finally, females might have a sensory bias
and be attracted to vitamin E because this could be a food
stimulus, indicating the presence of food, independently of the
male signal . Distinguishing between these scenarios requires
further experiments. However, it is likely that only high quality
males might allow investing high amounts of vitamin E into their
secretions and be able to attract females to their territories.
Therefore, we suggest that the cost of allocating vitamin E to
secretions, which should be differentially costly for different
individual males, may be a mechanism that confers reliability to
scent marks of green lizards and allows their evolution as sexual
signals. Nevertheless, we cannot exclude an alternative scenario
about the role of vitamin E supplementation. In theory, it might
be possible that the extra dietary vitamin E increased not only
the relative amount of vitamin E in the secretion, but the total
quantity of secretion itself too, and that female European green
lizards might be associated with larger amounts of secretion from
experimental males rather than with secretions with relatively
higher vitamin E content. However, the amount of femoral
secretion produced is under direct androgenic control in lizards,
such that androgen treated males have higher secretion rates
independently of the diet [reviewed in 13, 20]. Moreover,
chemosensory responses of female Iberian rock lizards to scent of
males or mixes of compounds seem related to the composition of
the chemical stimulus, rather than to the total quantity of the
chemical stimulus (19, unpublished data ), making the above
Sexual selection and female mate choice within it are widely
studies topics in a number of taxa . Surprisingly, such studies
on reptiles are scarce, despite the wide array of potential signals
(colorful ornaments, chemical signals, behavioral displays) that
reptiles, and especially lizards exhibit (e.g. [25,43–46]). Unlikely
in many taxa , female mate choice has rarely been reported
in lizards [47–48]. Mating seems to be under strict male control
in non-territorial lizards  and female mate choice is unlikely
to be important in such systems (but see ) where females
copulate with multiple males and have the potential to choose
only at the sperm level [47–48]. However, in lizards where males
are territorial (like the European green lizard) females have the
chance to choose their reproductive partner either according to
its own quality [35,41,45,51] or indirectly, according to the
quality of its territory . Further, considering visual vs.
chemical signals, females can choose both in the presence and
absence of males. The vitamin E content based female
preference reported here suggests that female European green
lizards can choose their potential reproductive partner in the
absence of it, however, we do not know if vitamin E levels reflect
the quality of the males, of their territories or both. A recent
study reported female mate preference based on nuptial throat
coloration (ultraviolet) in European green lizards . Hence, it
seems that females of this lizard species have multiple ways and
means to assess the quality of their potential reproductive
In summary, we found that the vitamin E content of the femoral
gland secretion of male European green lizards depends on their
food, and that females preferred to associate with male scents with
high vitamin E content. We suggest that the possible – male
quality dependent – cost of allocating vitamin E to secretions may
be a mechanism that confers reliability to scent marks of green
lizards and allows their evolution as sexual signals. This result –
together with a recent finding about visual female choice in the
same species  – suggests that female mate choice may be an
important agent of sexual selection in this species. Whether high
vitamin E levels in nature reflects quality of males or their
territories, or acts via conserving other signal molecules in the
secretion or by female sensory bias towards vitamin E remains to
be tested in the future.
We thank Ja ´nos To ¨ro ¨k for useful advice and support. We are highly
indebted to Katalin Bajer and Orsolya Molna ´r for their help in the
Conceived and designed the experiments: RK JM PL GH. Performed the
experiments: RK. Analyzed the data: RK JM GH. Contributed reagents/
materials/analysis tools: JM PL. Wrote the paper: RK JM PL GH.
Figure 2. Strength of female preference for male scent. Female
‘strength of preference’ was calculated for every male pair as the
difference in the mean proportion unmated female lizards (see text for
details) were observed at the areas containing chemical cues from size-
matched vitamin E supplemented vs. control male European green
lizards. Vitamin E difference is the difference in relative vitamin E
content of the femoral secretions of size-matched vitamin E supple-
mented vs. control males within a male pair.
Vitamin E as a Sexual Signal in Lizards
PLoS ONE | www.plosone.org4 April 2011 | Volume 6 | Issue 4 | e19410
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Vitamin E as a Sexual Signal in Lizards
PLoS ONE | www.plosone.org5 April 2011 | Volume 6 | Issue 4 | e19410